Science - USA (2022-02-11)

11 FEBRUARY 2022 • VOL 375 ISSUE 6581 615

CREDITS: (TOP GERD SCHROEDERTURK/MURDOCH UNIVERSITY; (BOTTOM LEFT AND MIDDLE FIONA MELDRUM; (BOTTOM RIGHT BODO WILTS/UNIVERSITY OF SALZBURG; ADAPTED BY K. FRANKLIN/

SCIENCE

SCIENCE science.org

By Stephen T. Hyde^1 and Fiona C. Meldrum^2

T

he growth and form of crystals in

vivo—biomineralization—challenge

many ideas about crystalline materi-

als. One typically pictures a crystal as a

sterile object with a regular geometric

form, but nature frequently challenges

this preconception. This is beautifully illus-

trated by the calcite plates (stereom) of echi-

noderms, which exhibit complex, sponge-like

morphologies and curved surfaces and yet

behave as single crystals. Extraordinarily, the

stereom of certain species is highly ordered.

Observations of the sea urchin Cidaris ru-

gosa more than six decades ago

( 1 ) identified a stereom remi-

niscent of one of the three sim-

plest triply periodic minimal

surfaces (TPMS), the so-called

P surface, with a lattice param-

eter four orders of magnitude

larger than that of calcite. On

page 647 of this issue, Yang et

al. ( 2 ) provide a new example

of a TPMS at this extreme

length scale. Detected in the

knobbly starfish Protoreaster

nodosus, the stereom resem-

bles another simple TPMS, the

D surface.

TPMS-related structures

have been reported in a va-

riety of living and nonliv-

ing systems, from soft liquid

crystalline assemblies to hard

wing scales and exoskeletons

in insects ( 3 ). The genesis and

stability of TPMS with lattice

parameters of up to ~100 nm

in vitro can be understood as a

relaxed soft membrane assem-

bly, which is the outcome of competing in-

teractions within the molecular constituents

of the membranes, e.g., lipids or copolymers

( 4 ). The three simplest TPMS geometries are

the gyroid (G), diamond (D), and primitive

(P), all of which have cubic symmetry (see

the figure). Microstructures related to the G

and D geometries have been found in biologi-

cal chitin assemblies, where they far exceed

the 100-nm threshold. These form the pho-

tonic crystals responsible for the iridescence

of butterfly wings and weevil carapaces ( 5 ).

The growth of such structures in the wing

scales of butterfly pupae is associated with

a particular cellular organelle known as the

smooth endoplasmic reticulum, which folds

to give a convoluted membrane whose form

is markedly similar to the G morphology ( 6 ).

Templating of the growing chitin crystal by a

TPMS-like soft membrane is thus a plausible,

though unproven, mechanism that explains

the formation of these microstructures.

Yang et al. investigated the structure of the

stereom formed by the starfish P. nodosus at

angstrom and higher length scales. In con-

trast to the sea-urchin C. rugosa, plates of P.

nodosus resemble the D surface and exhibit

a 30-μm lattice parameter, a measurement

made on the basis of the types and preva-

lence of structural defects compared with

the ideal D surface. These defects may ex-

plain why the structure responds to loading

in a way that is reminiscent of soft materials,

avoiding brittle fracture commonly associ-

ated with calcite. Some of that data suggest

microstructural tuning for biological fitness

during evolution. However, given the similar

defects in mesoporous and amorphous silica

grown within synthetic membranes with G

morphologies ( 7 ), this remains speculative.

Yang et al. reveal an extraordinary in-

terplay between the calcite structures at

micrometer and angstrom length scales of

cubic and rhombohedral symmetries, re-

spectively. Despite its atomic-scale crystal-

linity, the calcite fractures like glass, unlike

the precise cleavage planes exhibited by

geological calcite. This can be attributed to

the composite structure of biological calcite,

in which organic macromolecules are oc-

cluded within the crystal lattice. Further, as

proposed as early as the 1960s ( 8 ), it is now

accepted that these calcite biominerals are

better described as “mesocrystals,” composed

of space-filling arrays of calcite

nanoparticles, rather than true

single crystals ( 9 ). This struc-

ture is a direct consequence of

the crystallization mechanism,

whereby biogenic calcite often

forms through an amorphous

calcium carbonate (ACC) pre-

cursor phase. The shape of the

constituent ACC nanoparticles

is then preserved within the

product calcite. It is also con-

ceivable that the mesocrystal

ultrastructure enables the crys-

tal lattice to warp and follow

the shape of the skeletal sur-

face in some echinoderms ( 10 ).

These findings confirm the

extraordinary control that

biology achieves over crystal-

lization. Traditional models of

biomineralization emphasize

the role of soluble macromol-

ecules in directing crystal

morphologies. The D-type

TPMS can be considered as a

network of four-armed tetra-

pods. Calcite crystals with comparable tetra-

pod morphologies can be generated by using

soluble additives. Such a model is consistent

with the calcite shells of some dinoflagellates,

a type of phytoplankton ( 11 ), which are remi-

niscent of a disordered echinoderm stereom

but comprise multiple crystallites. Instead,

the echinoderm stereom is templated by an

organic matrix that defines its morphology.

This has been demonstrated in studies of sea

urchin larvae, in which mineralization be-

gins with the formation of a triradiate calcite

crystal (spicule). Culturing larvae under con-

ditions that change the shape of the organic

BIOPHYSICS

Starfish grow extraordinary crystals

Biomineralization in a starfish displays morphologically complex features

(^1) School of Chemistry, University of Sydney, Sydney, New
South Wales 2006, Australia.^2 School of Chemistry,
University of Leeds, Woodhouse Lane, Leeds, LS2 9JT, UK.
Email: [email protected]; [email protected]
10 μm
Sea urchin skeletal plate
with primitive-type structure
Primitive-type
10 μm
Calcite crystal
Diamond-type
1 μm
Buttery scale with
gyroid-type structure
Gyroid-type
Three simplest triple periodic minimal surfaces
Although triply periodic minimal surfaces (TPMS) have been observed in the natural
world, examples of TPMS with large length scales in living organisms are extremely
rare. Researchers have now identified a diamond-type TPMS in the calcium carbonate
skeletal elements of the knobbly starfish. This raises questions about the mechanisms
by which organisms sculpt the morphologies of these biominerals.